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Limited Effects of a Keystone Species: Trends of Sea Otters and Kelp Forests at the Semichi Islands, Alaska

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Limited Effects of a Keystone Species: Trends of Sea Otters and Kelp Forests at the Semichi Islands, Alaska MARINE ECOLOGY PROGRESS SERIES Vol. 199: 271-280,2000 Published June 26 Mar Ecol Prog Ser I Limited effects of a keystone species: trends of sea otters and kelp forests at the Semichi Islands, Alaska Brenda Konar* U.S. Geological Survey, University of California, Santa Cruz, California, USA ABSTRACT: Sea otters are well known as a keystone species because of their ability to transform sea urchin-dominated communities into kelp-dominated communities by preying on sea urchins and thus reducing the intensity of herbivory. After being locally extinct for more than a century, sea otters re-col- onized the Sernichi Islands in the Aleutian Archipelago, Alaska in the early 1990s. Here, otter popula- tions increased to about 400 individuals by 1994, but rapidly declined to about 100 by 1997. Roughly 7 yr after initial otter re-colonization, there were only marginal changes in sea urchm biomass, mean maximum test size, and kelp density. These small changes may be the first steps in the cascahng effects on community structure typically found with the invasion of a keystone species. However, no wholesale change in community structure occurred following re-colonization and growth of the sea otter population. Instead, this study describes a transition state and identifies factors such as keystone species density and residence time that can be important in dictating the degree to which otter effects are manifested. KEY WORDS: Community structure . Trophic interactions . Urchin barrens . Enhydra lutris . Strongy- locentrotuspolyacanthus . Alaria fistulosa INTRODUCTION proportionately large relative to its abundance, and thus keystones are usually rare (Power et al. 1996). The various species that belong to an ecological Dominant species are cominonly assumed to be of community can assume diverse roles within the food primary importance according to the bottom-up view web and conlpetitive hierarchy, and will always rank of trophic interactions, which considers lower-level very differently in their importance in structuring the producers to have a primary role in structuring com- community (Paine 1992, Mills et al. 1993, McCann et munities (see Hunter & Price 1992, Power 1992 for al. 1998).While there is clearly a gradient in the impor- reviews). This, however, is not always the case. A top- tance of species, a small number of species is often down view of trophic interactions may also charac- easily identified as occupying positions of particularly terize dominants as playing a controlling role in com- strong influence on community structure. These spe- munity structure. This is illustrated in systems where cies often fill 1 of 2 mutually exclusive roles: dominant herbivores or omnivores are not limited by predation. or keystone. Dominant species are ones in which den- In this case, animal abundances can increase, such that sities or total biomass are very high, and for which these organisms become important dominants, sup- community influence is a direct result of abundance. A planting the controlling role of plants. Classic exam- keystone species is defined as one whose effect is dis- ples of such dominant species are sea urchins (Andrew & Underwood 1993) and mussels (Paine 1974). In some 'Present address: School of Fisheries and Ocean Sciences, systems, sea urchins can become so abundant that they University of Alaska Fairbanks, PO Box 757220, Fairbanks, overgraze attached plants in kelp forests, leaving what Alaska 99775-7220. USA. E-md: [email protected] are commonly termed 'barren grounds' (areas devoid O Inter-Research 2000 Resale of full article not permitted 232 Mar Ecol Prog Ser of macroalgae; Arnold 1976, Chapman 1981, Schiel fects exerted by a keystone species on community 1982, Dean et al. 1984, Harrold & Pearse 1987, Watan- structure do not depend on high densities, but the ex- abe & Harrold 1991), while mussels can form mono- tent to which community-wide effects of keystone spe- cultures by outcompeting other sessile organisms for cies depend on the attainment of some critical density space (Paine 1974, Robles et al. 1995). has not been carefully evaluated. Here these issues are Members of a second group of important species addressed by examining the keystone role of sea otters have been labeled as keystones (sensu Paine 1969).By Enhydra lutris in kelp forest communities in the Semi- current definition, keystone species are comparatively chi Islands of the Aleutian Archipelago, Alaska. rare in the communities in whch they reside (Power et The Semichi lsland group consists of 3 islands, al. 1996). Keystone species have been identified in Shemya, Nizki and Alaid (Fig. 1). Shemya Island numerous ecosystems and at all trophic levels (see (52"43'N, 174"07'E) is the furthest east and largest of Mills et al. 1993, Power et al. 1996 for reviews). In these 3 islands. The island has a shoreline of 22 km. communities controlled by top-down forces, the key- Nizki and Alaid are slightly smaller than Shemya and stones are often apex predators. These predators con- are attached to each other by a sand bar at low tide. trol their prey (often herbivores), which otherwise act There is approximately a 1.5 km wide channel as dominants, thereby exerting strong effects on com- between the islands of Shemya and Nizki. All 3 of munity structure. The influence of keystone species is these islands are exposed directly to swell and wave best seen by observing systems in which the key- action from the Bering Sea to the north and the Pacific stone's population status is in flux, either through pur- Ocean to the south. poseful or fortuitous experiments. In this situation, a rise or fall in the keystone population abundance can cause cascading effects on its prey, their food species, THE ALEUTIAN NEARSHORE ECOSYSTEM and ultimately on the entire food chain. (Fretwell 1987). There has been a tendency in the ecological litera- Sea otter population status ture to apply the labels 'dominant' or 'keystone' to spe- cies wherever they occur. In fact, the evidence from Sea otters were once abundantly distributed in nature indicates that these roles are highly context coastal waters across the Pacific rim from Japan to cen- dependent (Foster 1990, Menge et al. 1994, Dean et al. tral Baja, California (Kenyon 1969).By the early 1900s, 2000). The ability of a given species to exert a strong the Pacific maritime fur trade had caused the local influence on a community structure (as either a domi- extinction of sea otters in most of the Aleutian Islands. nant or a keystone) is dependent upon community Following their protection by the International Fur composition and can be particularly sensitive to condi- Seal Treaty in 1911, sea otters remnant at Rat Island tions. For example, sea urchins may be dominant and recolonized the Rat Island group, and apparently capable of overgrazing attached macroalgae in one area while in another area or at a different time they have no dominant effect because of variation in factors such as food availability (Harrold & Reed 1985), water movement (Ebeling et al. 1985), or population den- sity (Andrew & Underwood 1993). Similar context- 60" 'lands dependent variation in the keystone effects of seastar (Menge et al. 1994) and lobster (Robles 1997) preda- 'S* ,....a tion on intertidal mussels has been demonstrated for 160" 140" changes in wave exposure and sedimentation. With changes in these conditions, a potentially important ---$,.'g species may quickly change from a minor player to one = E actively controlling community structure, and vice . versa. While such context dependence is recognized for Pacific Ocean Nizki 0. C some species, few studies have quantitatively ad- Shemya dressed the factors that may limit the effect of a key- stone species on community structure (except see Dean et al. 2000). In particular, it is not clear how sensitive the Fig. 1. Map of the Semichi Islands showing the location of influences of keystone species are to internal factors Alaid, Nizlu, and Shemya with dive iocations (0). inset: map such as the amount of time a species has been present of Alaska showing the location of the Semichi Islands and in a community or to its density. By definition, the ef- neighboring island groups Konar: Effects of sea 01 tters as a keystone species 273 reached carrying capacity throughout this area by the cluding the rock jingle Pododesmus macroschisma; De- 1950s. The Near Island group, about 225 km further shayes), chitons (including Katharina tunicata; Wood, west, did not become re-occupied until the mid-1960s, and Cryptochiton stelleri; Middendorf), limpets, crabs when a small number of sea otters re-colonized Attu and seastars are all common inhabitants in this subtidal Island. The sea otter population at Attu grew rapidly community. All of the above are known prey items of the through the 1970s and 1980s (Estes 1990). Another sea otter in the Aleutians particularly when sea urchins Near Island, Agattu, was recolonized in the early are small or scarce (Estes et al. 1981, VanBlaricom & 1980s. The Semichi Islands, approximately 30 km to Estes 1988). the northeast, were recolonized in the early 1990s. Rocky subtidal habitats are patchy around the Semi- In the Aleutian Islands, sea otters are considered chi Islands. This leads to a patch mosaic of kelp forests keystone species because of their influence as preda- and barren grounds. Course-grained sand surrounds tors in kelp forest ecosystems (Estes & Palmisano 1974, most of these rocky outcroppings. No macroinverte- Estes et al. 1978, Estes & Duggins 1995), where they brates were found in these sandy areas (author's pers. can eat approximately 15 to 20% of their body mass obs.) because of the overall exposure to swell and cur- daily (Kenyon 1969). Sea urchins Strongylocentrotus rents. Also, no sea otters were ever observed foraging polyacanthus are a preferred prey of sea otters (Estes in these areas, probably due to the lack of inverte- et al.
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